Functional Connectivity between the Cerebellum and Somatosensory Areas Implements the Attenuation of Self-Generated Touch

Abstract

Since the early 1970s, numerous behavioral studies have shown that self-generated touch feels less intense and less ticklish than the same touch applied externally. Computational motor control theories have suggested that cerebellar internal models predict the somatosensory consequences of our movements and that these predictions attenuate the perception of the actual touch. Despite this influential theoretical framework, little is known about the neural basis of this predictive attenuation. This is due to the limited number of neuroimaging studies, the presence of conflicting results about the role and the location of cerebellar activity, and the lack of behavioral measures accompanying the neural findings. Here, we combined psychophysics with fMRI to detect the neural processes underlying somatosensory attenuation in male and female healthy human participants. Activity in bilateral secondary somatosensory areas was attenuated when the touch was presented during a self-generated movement (self-generated touch) than in the absence of movement (external touch). An additional attenuation effect was observed in the cerebellum that is ipsilateral to the passive limb receiving the touch. Importantly, we further found that the degree of functional connectivity between the ipsilateral cerebellum and the contralateral primary and bilateral secondary somatosensory areas was linearly and positively related to the degree of behaviorally assessed attenuation; that is, the more participants perceptually attenuated their self-generated touches, the stronger this corticocerebellar coupling. Collectively, these results suggest that the ipsilateral cerebellum is fundamental in predicting self-generated touch and that this structure implements somatosensory attenuation via its functional connectivity with somatosensory areas.

Action enhances predicted touch

“…Furthermore, it is essential to note that findings of reduced somatosensory (Blakemore et al, 1998;Kilteni & Ehrsson, 2020;Shergill et al, 2013) or visual (Kontaris et al, 2009;Stanley & Miall, 2007) neural response when perceiving expected action outcomesfrequently taken to support attenuation theoriesmay not be reflective of predictive downweighting processes.…”

“…For example, if we lift a cup of coffee that is lighter than expected, attenuated processing of expected signals (e.g., touch on our fingertips) will allow dedicated processing of unexpected events (e.g., accelerating motion of the cup) to allow swift updating of our beliefs about the environment (e.g., the weight of the cup) and support corrective action to avoid spillage. These downweighting mechanisms are invoked to explain that self-produced tactile sensations generate lower activity in bilateral secondary somatosensory cortex (Blakemore et al, 1998;Kilteni & Ehrsson, 2020;Shergill et al, 2013Shergill et al, , 2014, and are perceived to be less intense (Bays et al, 2005(Bays et al, , 2006Kilteni et al, 2019;Kilteni & Ehrsson, 2017;Shergill et al, 2003;Wolpe et al, 2016Wolpe et al, , 2018, than externallyproduced forces. This theory also provides an explanation for why it is difficult to tickle oneself (Blakemore et al, 1998).…”

“…Additionally, predictive influences on perception may be mediated by different neural mechanisms that exhibit different functions. Specifically, tactile attenuation during action is thought to be dependent on the degree of connectivity between secondary somatosensory cortex and the cerebellum (Kilteni & Ehrsson, 2020), whereas prediction in the visual domain is thought to be mediated by hippocampal representation (Kok et al, 2020;Kok & Turk-Browne, 2018). Therefore, in principle cerebellar predictions may attenuate sensation, whereas hippocampal predictions may sharpen it.…”

Prosthesis embodiment and attenuation of prosthetic touch in upper limb amputees – a proof-of-concept study

“…However, future studies should substantiate our findings by the assessment of behavioral (e.g., Bays et al, 2005) or neurophysiological measures (e.g., Kilteni & Ehrsson, 2020;Zeller, Litvak, Friston, & Classen, 2015), the latter which might also reveal the proposed interplay between the cerebellum and higher-order cortical regions. This kind of forward and backward dynamics is for which dynamic causal modelling (DCM; Friston, Harrison, & Penny, 2003) has been developed, an analysis technique for testing effective connectivity of reciprocal self-organized systems.…”

Motor-evoked neural responses in auditory cortex are associated with improved sensitivity to self-generated sounds

“…For example, in the auditory domain, perceived loudness is typically attenuated for salient self-generated sounds compared to identical sounds produced by someone else (e.g., Weiss et al, 2011). Similarly, perceived tactile pressure is lower when it is applied by the perceiver vs. by an external source (Blakemore et al, 1998;Kilteni and Ehrsson, 2020;Shergill et al, 2005;Walsh et al, 2011), an effect also associated with the phenomenon that one cannot tickle oneself (Blakemore et al, 1999).…”